Neuroanatomy of the crocodylian Tomistoma dowsoni from the Miocene of North Africa provides insights into the evolutionary history of gavialoids

Abstract

The interrelationships of the extant crocodylians Gavialis gangeticus and Tomistoma schlegelii have been historically disputed. Whereas molecular analyses indicate a sister taxon relationship between these two gavialoid species, morphological datasets typically place Gavialis as the outgroup to all other extant crocodylians. Recent morphological-based phylogenetic analyses have begun to resolve this discrepancy, recovering Gavialis as the closest living relative of Tomistoma; however, several stratigraphically early fossil taxa are recovered as closer to Gavialis than Tomistoma, resulting in anomalously early divergence timings. As such, additional morphological data might be required to resolve these remaining discrepancies. 'Tomistoma' dowsoni is an extinct species of gavialoid from the Miocene of North Africa. Utilising CT scans of a near-complete, referred skull, we reconstruct the neuroanatomy and neurosensory apparatus of 'Tomistoma' dowsoni. Based on qualitative and quantitative morphometric comparisons with other crocodyliforms, the neuroanatomy of 'Tomistoma' dowsoni is characterised by an intermediate morphology between the two extant gavialoids, more closely resembling Gavialis. This mirrors the results of recent studies based on the external anatomy of these three species and other fossil gavialoids. Several neuroanatomical features of these species appear to reflect ecological and/or phylogenetic signals. For example, the 'simple' morphology of their neurosensory apparatus is broadly similar to that of other long and narrow-snouted (longirostrine), aquatic crocodyliforms. A dorsoventrally short, anteroposteriorly long endosseous labyrinth is also associated with longirostry. These features indicate that snout and skull morphology, which are themselves partly constrained by ecology, exert an influence on neuroanatomical morphology, as has also been recognised in birds and turtles. Conversely, the presence of a pterygoid bulla in Gavialis and several extinct gavialoids, and its absence in Tomistoma schlegelii, could be interpreted as a phylogenetic signal of crocodylians more closely related to Gavialis than to Tomistoma. Evaluation of additional fossil gavialoids will be needed to further test whether these and other neuroanatomical features primarily reflect a phylogenetic or ecological signal. By incorporating such previously inaccessible information of extinct and extant gavialoids into phylogenetic and macroecological studies, we can potentially further constrain the clade's interrelationships, as well as evaluate the timing and ecological association of the evolution of these neuroanatomical features. Finally, our study supports recent phylogenetic analyses that place 'Tomistoma' dowsoni as being phylogenetically closer to Gavialis gangeticus than to Tomistoma schlegelii, indicating the necessity of a taxonomic revision of this fossil species.

Keywords: Tomistominae; computed tomography; crocodylian; ecomorphology; gharial; morphometrics neuroanatomy.

FIGURE 1

(a) Isosurface rendering of the skull of ‘Tomistoma’ dowsoni based on NHMUK PV R 4769; (b) reconstruction of the neuroanatomy and neurosensory apparatus of ‘Tomistoma’ dowsoni; (c) isosurface rendering of the skull of Gavialis gangeticus based on FLMNH UF 118998; (d) reconstruction of the neuroanatomy and neurosensory apparatus of Gavialis gangeticus; (e) isosurface rendering of the skull of Tomistoma schlegelii based on TMM M6342; (f) reconstruction of the neuroanatomy and neurosensory apparatus of Tomistoma schlegelii. Scale bars = 50 mm.

FIGURE 2

The neuroanatomy of ‘Tomistoma’ dowsoni (NHMUK PV R 4769) in dorsal, left lateral and ventral views. Abbreviations: CCA, cerebral carotid artery; EC, external choana; ED, endosseous labyrinth; END, encephalic endocast; NC, nasal cavity; NPD, nasopharyngeal duct; OR, olfactory region; PNS, paranasal sinus; VC, neurovascular canal. Scale bar = 10 mm.

FIGURE 3

The neuroanatomy of Gavialis gangeticus (FLMNH UF 118998) in dorsal, left lateral and ventral views. Abbreviations: BL, pterygoid bulla; CCA, cerebral carotid artery; EC, external choana; ED, endosseous labyrinth; END, endocast; IC, internal choana; NC, nasal cavity; NLD, nasolacrimal duct; NPD, nasopharyngeal duct; OR, olfactory region; PNS, paranasal sinus; VC, neurovascular canal. Scale bar = 10 mm.

FIGURE 4

The neuroanatomy of Tomistoma schlegelii (TMM M6342) in dorsal, left lateral and ventral views. Abbreviations: CCA, cerebral carotid artery; EC, external choana; ED, endosseous labyrinth; END, endocast; IC, internal choana; NC, nasal cavity; NLD, nasolacrimal duct; NPD, nasopharyngeal duct; OR, olfactory region; PNS, paranasal sinus; VC, neurovascular canal. Scale bar = 10 mm.

FIGURE 5

The endocast of ‘Tomistoma’ dowsoni (NHMUK PV R 4769) in dorsal, left lateral and ventral views. Abbreviations: CCA, cerebral carotid artery; CER, cerebrum; DLS, dorsal longitudinal sinus; MO, medulla oblongata; OB, olfactory bulb; OT, olfactory tract. Scale bar = 10 mm.

FIGURE 6

The endocast of Gavialis gangeticus (FLMNH UF 118998) in dorsal, left lateral and ventral views. Abbreviations: CCA, cerebral carotid artery; CER, cerebrum; DLS, dorsal longitudinal sinus; MO, medulla oblongata; OB, olfactory bulb; OT, olfactory tract. Scale bar = 10 mm.

FIGURE 7

The endocast of Tomistoma schlegelii (TMM M6342) in dorsal, left lateral and ventral views. Abbreviations: CCA, cerebral carotid artery; CER, cerebrum; DLS, dorsal longitudinal sinus; MO, medulla oblongata; OB, olfactory bulb; OT, olfactory tract. Scale bar = 10 mm.

FIGURE 8

Endosseous labyrinths of A) ‘Tomistoma’ dowsoni (NHMUK PV R 4769), Gavialis gangeticus (FLMNH UF 118998), and Tomistoma schlegelii (TMM M6342) in anterior, dorsal and posterior views. Abbreviations: ASC, anterior semi‐circular canal; CC, common crus; CD, cochlear duct; LSC, lateral semi‐circular canal; PSC, posterior semi‐circular canal. Scale bar = 10 mm.

FIGURE 9

Principal component analysis (PCA) showing the variation in the shape of the endosseous labyrinth in 20 species of Crocodylomorpha. (a) shows the variation between PC1 versus PC2, (b) shows the variation between PC1 versus PC3. Skull morphology is highlighted in blue for longirostrine taxa, pink for mesorostrine taxa and red for brevirostrine taxa (see Table 3). (c) shows the shape variation in PC1, d) variation in PC2 and (e) variation in PC3. Arrows indicate the direction of change in the endosseous labyrinth. Skull silhouettes in (a) Tomistoma schlegelii (TMM M6342) and Cricosaurus araucanensis (MLP 72‐IV‐7‐1) (blue); Crocodylus rhombifer (NMB AB50.0171) and Osteolaemus tetraspis (FMNH 98386) (pink); Junggarsuchus sloani (IVPP V14010) and Mourasuchus arendsi (MLP 73‐IV‐15‐9) (red); (b) ‘Tomistoma’ dowsoni (NHMUK PV R 4769) and Gunggamarandu maunala (QMF 548) (blue); Crocodylus rhombifer (NMB AB50.0171) (pink); Mourasuchus arendsi (MLP 73‐IV‐15‐9) (red).